Treatment of spontaneously hypertensive rats with rosiglitazone ameliorates cardiovascular pathophysiology via antioxidant mechanisms in the vasculature

American Journal of Physiology - Endocrinology and Metabolism

Volumn 297, Issue 3, 2009, Pages

  Potenza, Maria A ^a   Gagliardi, Sara ^a   De Benedictis, Leonarda ^a   Zigrino, Addolorata ^a   Tiravanti, Edy ^a   Colantuono, Giuseppe ^a   Federici, Antonio ^a   Lorusso, Loredana ^a   Benagiano, Vincenzo ^a   Quon, Michael J ^b   Montagnani, Monica ^a  

^a UNIVERSITY OF BARI   (Italy)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

Oxidative stress

Indexed keywords

3 NITROTYROSINE; 8 ISOPROSTAGLANDIN F2 ALPHA; APOCYNIN; INSULIN; N(G),N(G) DIMETHYLARGININE; PROTEIN P22; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; ROSIGLITAZONE; SUPEROXIDE DISMUTASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; AORTA; ARTICLE; CARDIOVASCULAR FUNCTION; CELL CULTURE; CONTROLLED STUDY; DRUG MECHANISM; ENDOTHELIUM CELL; ENZYME ACTIVITY; HEART INFARCTION; HEART MUSCLE ISCHEMIA; HYPERTENSION; INSULIN BLOOD LEVEL; INSULIN SENSITIVITY; ISOLATED HEART; LIPID PEROXIDATION; MALE; MESENTERY BLOOD FLOW; NONHUMAN; OXIDATIVE STRESS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REPERFUSION INJURY; SPONTANEOUSLY HYPERTENSIVE RAT; SYSTOLIC BLOOD PRESSURE; VASCULAR ENDOTHELIUM; VASCULARIZATION;

ANIMALS; ANTIOXIDANTS; BLOOD VESSELS; CARDIOVASCULAR SYSTEM; CATTLE; CELLS, CULTURED; DRUG EVALUATION, PRECLINICAL; HYPERTENSION; MALE; NADPH OXIDASE; OXIDATIVE STRESS; PHENOTYPE; RATS; RATS, INBRED SHR; RATS, INBRED WKY; SUPEROXIDE DISMUTASE; THIAZOLIDINEDIONES;

EID: 69049111960     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00291.2009     Document Type: Article

References (77)

1. Adler S, Huang H. Oxidant stress in kidneys of spontaneously hypertensive rats involves both oxidase overexpression and loss of extracellular superoxide dismutase. Am J Physiol Renal Physiol 287: F907-F913, 2004.
2. Anderson EJ, Lustig ME, Boyle KE, Woodlief TL, Kane DA, Lin CT, Price JW III, Kang L, Rabinovitch PS, Szeto HH, Houmard JA, Cortright RN, Wasserman DH, Neufer PD. Mitochondrial H2O2 emission and cellular redox state link excess fat intake to insulin resistance in both rodents and humans. J Clin Invest 2009 Feb 2. [Epub ahead of print].
3. Bagi Z, Koller A, Kaley G. PPARγ activation, by reducing oxidative stress, increases NO bioavailability in coronary arterioles of mice with type 2 diabetes. Am J Physiol Heart Circ Physiol 286: H742-H748, 2004.
4. Beswick RA, Dorrance AM, Leite R, Webb RC. NADH/NADPH oxidase and enhanced superoxide production in the mineralocorticoid hypertensive rat. Hypertension 38: 1107-1111, 2001.
5. Brownlee M. The pathobiology of diabetic complications: a unifying mechanism. Diabetes 54: 1615-1625, 2005.
6. Burdi R, Rolland JF, Fraysse B, Litvinova K, Cozzoli A, Giannuzzi V, Liantonio A, Camerino GM, Sblendorio V, Capogrosso RF, Palmieri B, Andreetta F, Confalonieri P, De Benedictis L, Montagnani M, De Luca A. Multiple pathological events in exercised dystrophic mdx mice are targeted by pentoxifylline: outcome of a large array of in vivo and ex vivo tests. J Appl Physiol 106: 1311-1324, 2009.
7. Calkin AC, Forbes JM, Smith CM, Lassila M, Cooper ME, Jandeleit-Dahm KA, Allen TJ. Rosiglitazone attenuates atherosclerosis in a model of insulin insufficiency independent of its metabolic effects. Arterioscler Thromb Vasc Biol 25: 1903-1909, 2005.
8. Calnek DS, Mazzella L, Roser S, Roman J, Hart CM. Peroxisome proliferator-activated receptor gamma ligands increase release of nitric oxide from endothelial cells. Arterioscler Thromb Vasc Biol 23: 52-57, 2003.
9. Cefalu WT. Glycemic targets and cardiovascular disease. N Engl J Med 358: 2633-2635, 2008.
10. Ceolotto G, Gallo A, Papparella I, Franco L, Murphy E, Iori E, Pagnin E, Fadini GP, Albiero M, Semplicini A, Avogaro A. Rosiglitazone reduces glucose-induced oxidative stress mediated by NAD(P)H oxidase via AMPK-dependent mechanism. Arterioscler Thromb Vasc Biol 27: 2627-2633, 2007.
11. Ceradini DJ, Yao D, Grogan RH, Callaghan MJ, Edelstein D, Brownlee M, Gurtner GC. Decreasing intracellular superoxide corrects defective ischemia-induced new vessel formation in diabetic mice. J Biol Chem 283: 10930-10938, 2008.
12. Ceriello A, Motz E. Is oxidative stress the pathogenic mechanism underlying insulin resistance, diabetes, and cardiovascular disease? The common soil hypothesis revisited. Arterioscler Thromb Vasc Biol 24: 816-823, 2004.
13. Cifuentes ME, Rey FE, Carretero OA, Pagano PJ. Upregulation of p67(phox) and gp91(phox) in aortas from angiotensin II-infused mice. Am J Physiol Heart Circ Physiol 279: H2234-H2240, 2000.
14. Collins AR, Lyon CJ, Xia X, Liu JZ, Tangirala RK, Yin F, Boyadjian R, Bikineyeva A, Pratico D, Harrison DG, Hsueh WA. Age-accelerated atherosclerosis correlates with failure to upregulate antioxidant genes. Circ Res 104: e42-54, 2009.
15. Dluhy RG, McMahon GT. Intensive glycemic control in the ACCORD and ADVANCE trials. N Engl J Med 358: 2630-2633, 2008.
16. Dobrian AD, Schriver SD, Khraibi AA, Prewitt RL. Pioglitazone prevents hypertension and reduces oxidative stress in diet-induced obesity. Hypertension 43: 48-56, 2004.
17. Duckworth W, Abraira C, Moritz T, Reda D, Emanuele N, Reaven PD, Zieve FJ, Marks J, Davis SN, Hayward R, Warren SR, Goldman S, McCarren M, Vitek ME, Henderson WG, Huang GD. Glucose control and vascular complications in veterans with type 2 diabetes. N Engl J Med 360: 129-139, 2009.
18. Ferdinandy P, Schulz R, Baxter GF. Interaction of cardiovascular risk factors with myocardial ischemia/reperfusion injury, preconditioning, and postconditioning. Pharmacol Rev 59: 418-458, 2007.
19. Ford ES, Mokdad AH, Giles WH, Brown DW. The metabolic syndrome and antioxidant concentrations: findings from the Third National Health and Nutrition Examination Survey. Diabetes 52: 2346-2352, 2003.
20. Fortuno A, San Jose G, Moreno MU, Beloqui O, Diez J, Zalba G. Phagocytic NADPH oxidase overactivity underlies oxidative stress in metabolic syndrome. Diabetes 55: 209-215, 2006.
21. Gerstein HC, Miller ME, Byington RP, Goff DC Jr, Bigger JT, Buse JB, Cushman WC, Genuth S, Ismail-Beigi F, Grimm RH Jr, Probstfield JL, Simons-Morton DG, and Friedewald WT. Effects of intensive glucose lowering in type 2 diabetes. N Engl J Med 358: 2545-2559, 2008.
22. Goya K, Sumitani S, Otsuki M, Xu X, Yamamoto H, Kurebayashi S, Saito H, Kouhara H, Kasayama S. The thiazolidinedione drug troglitazone up-regulates nitric oxide synthase expression in vascular endothelial cells. J Diabetes Complications 20: 336-342, 2006.
23. Guzik TJ, Harrison DG. Vascular NADPH oxidases as drug targets for novel antioxidant strategies. Drug Discov Today 11: 524-533, 2006.
24. Hansel B, Giral P, Nobecourt E, Chantepie S, Bruckert E, Chapman MJ, Kontush A. Metabolic syndrome is associated with elevated oxidative stress and dysfunctional dense high-density lipoprotein particles displaying impaired antioxidative activity. J Clin Endocrinol Metab 89: 4963-4971, 2004.
25. Heumuller S, Wind S, Barbosa-Sicard E, Schmidt HH, Busse R, Schroder K, Brandes RP. Apocynin is not an inhibitor of vascular NADPH oxidases but an antioxidant. Hypertension 51: 211-217, 2008.
26. Hwang J, Kleinhenz DJ, Lassegue B, Griendling KK, Dikalov S, Hart CM. Peroxisome proliferator-activated receptor-γ ligands regulate endothelial membrane superoxide production. Am J Physiol Cell Physiol 288: C899-C905, 2005.
27. Hwang J, Kleinhenz DJ, Rupnow HL, Campbell AG, Thule PM, Sutliff RL, Hart CM. The PPARgamma ligand, rosiglitazone, reduces vascular oxidative stress and NADPH oxidase expression in diabetic mice. Vascul Pharmacol 46: 456-462, 2007.
28. Ide T, Tsutsui H, Kinugawa S, Suematsu N, Hayashidani S, Ichikawa K, Utsumi H, Machida Y, Egashira K, Takeshita A. Direct evidence for increased hydroxyl radicals originating from superoxide in the failing myocardium. Circ Res 86: 152-157, 2000.
29. Iglarz M, Touyz RM, Amiri F, Lavoie MF, Diep QN, Schiffrin EL. Effect of peroxisome proliferator-activated receptor-alpha and -gamma activators on vascular remodeling in endothelin-dependent hypertension. Arterioscler Thromb Vasc Biol 23: 45-51, 2003.
30. 2+-superoxide dismutase and decrease p22phox message expressions in primary endothelial cells. Metabolism 50: 3-11, 2001.
31. Katakam PV, Tulbert CD, Snipes JA, Erdos B, Miller AW, Busija DW. Impaired insulin-induced vasodilation in small coronary arteries of Zucker obese rats is mediated by reactive oxygen species. Am J Physiol Heart Circ Physiol 288: H854-H860, 2005.
32. Katz A, Nambi SS, Mather K, Baron AD, Follmann DA, Sullivan G, Quon MJ. Quantitative insulin sensitivity check index: a simple, accurate method for assessing insulin sensitivity in humans. J Clin Endocrinol Metab 85: 2402-2410, 2000.
33. Kerr S, Brosnan MJ, McIntyre M, Reid JL, Dominiczak AF, Hamilton CA. Superoxide anion production is increased in a model of genetic hypertension: role of the endothelium. Hypertension 33: 1353-1358, 1999.
34. Kim JA, Montagnani M, Koh KK, Quon MJ. Reciprocal relationships between insulin resistance and endothelial dysfunction: molecular and pathophysiological mechanisms. Circulation 113: 1888-1904, 2006.
35. Koh KK, Han SH, Quon MJ. Inflammatory markers and the metabolic syndrome: insights from therapeutic interventions. J Am Coll Cardiol 46: 1978-1985, 2005.
36. Koh KK, Oh PC, Quon MJ. Does reversal of oxidative stress and inflammation provide vascular protection? Cardiovasc Res 81: 649-659, 2009.
37. Koh KK, Quon MJ, Han SH, Ahn JY, Jin DK, Kim HS, Kim DS, Shin EK. Vascular and metabolic effects of combined therapy with ramipril and simvastatin in patients with type 2 diabetes. Hypertension 45: 1088-1093, 2005.
38. Koh KK, Quon MJ, Han SH, Chung WJ, Ahn JY, Seo YH, Kang MH, Ahn TH, Choi IS, Shin EK. Additive beneficial effects of losartan combined with simvastatin in the treatment of hypercholesterolemic, hypertensive patients. Circulation 110: 3687-3692, 2004.
39. Koh KK, Quon MJ, Han SH, Lee Y, Kim SJ, Koh Y, Shin EK. Distinct vascular and metabolic effects of different classes of anti-hypertensive drugs. Int J Cardiol 2008 Dec 5. [Epub ahead of print.]
40. Krumholz HM, Lee TH. Redefining quality-implications of recent clinical trials. N Engl J Med 358: 2537-2539, 2008.
41. Lago RM, Singh PP, Nesto RW. Congestive heart failure and cardiovascular death in patients with prediabetes and type 2 diabetes given thiazolidinediones: a meta-analysis of randomised clinical trials. Lancet 370: 1129-1136, 2007.
42. Lee S, Muniyappa R, Yan X, Chen H, Yue LQ, Hong EG, Kim JK, Quon MJ. Comparison between surrogate indexes of insulin sensitivity and resistance and hyperinsulinemic euglycemic clamp estimates in mice. Am J Physiol Endocrinol Metab 294: E261-E270, 2008.
43. Lum H, Roebuck KA. Oxidant stress and endothelial cell dysfunction. Am J Physiol Cell Physiol 280: C719-C741, 2001.
44. Mallat Z, Philip I, Lebret M, Chatel D, Maclouf J, Tedgui A. Elevated levels of 8-iso-prostaglandin F2alpha in pericardial fluid of patients with heart failure: a potential role for in vivo oxidant stress in ventricular dilatation and progression to heart failure. Circulation 97: 1536-1539, 1998.
45. Mazzone T, Meyer PM, Feinstein SB, Davidson MH, Kondos GT, D'Agostino RB, Sr., Perez A, Provost JC, Haffner SM. Effect of pioglitazone compared with glimepiride on carotid intima-media thickness in type 2 diabetes: a randomized trial. JAMA 296: 2572-2581, 2006.
46. Mersmann J, Tran N, Zacharowski PA, Grotemeyer D, Zacharowski K. Rosiglitazone is cardioprotective in a murine model of myocardial I/R. Shock 30: 64-68, 2008.
47. Montagnani M, Golovchenko I, Kim I, Koh GY, Goalstone ML, Mundhekar AN, Johansen M, Kucik DF, Quon MJ, Draznin B. Inhibition of phosphatidylinositol 3-kinase enhances mitogenic actions of insulin in endothelial cells. J Biol Chem 277: 1794-1799, 2002.
48. Moore KJ, Rosen ED, Fitzgerald ML, Randow F, Andersson LP, Altshuler D, Milstone DS, Mortensen RM, Spiegelman BM, Freeman MW. The role of PPAR-gamma in macrophage differentiation and cholesterol uptake. Nat Med 7: 41-47, 2001.
49. Muniyappa R, Lee S, Chen H, Quon MJ. Current approaches for assessing insulin sensitivity and resistance in vivo: advantages, limitations, and appropriate usage. Am J Physiol Endocrinol Metab 294: E15-E26, 2008.
50. Muniyappa R, Montagnani M, Koh KK, Quon MJ. Cardiovascular actions of insulin. Endocr Rev 28: 463-491, 2007.
51. Nakamura T, Yamamoto E, Kataoka K, Yamashita T, Tokutomi Y, Dong YF, Matsuba S, Ogawa H, Kim-Mitsuyama S. Pioglitazone exerts protective effects against stroke in stroke-prone spontaneously hypertensive rats, independently of blood pressure. Stroke 38: 3016-3022, 2007.
52. Nakane H, Miller FJ Jr, Faraci FM, Toyoda K, and Heistad DD. Gene transfer of endothelial nitric oxide synthase reduces angiotensin II-induced endothelial dysfunction. Hypertension 35: 595-601, 2000.
53. Nascimento NR, Lessa LM, Kerntopf MR, Sousa CM, Alves RS, Queiroz MG, Price J, Heimark DB, Larner J, Du X, Brownlee M, Gow A, Davis C, Fonteles MC. Inositols prevent and reverse endothelial dysfunction in diabetic rat and rabbit vasculature metabolically and by scavenging superoxide. Proc Natl Acad Sci USA 103: 218-223, 2006.
54. Nissen SE, Wolski K. Effect of rosiglitazone on the risk of myocardial infarction and death from cardiovascular causes. N Engl J Med 356: 2457-2471, 2007.
55. Nolan JJ, Ludvik B, Beerdsen P, Joyce M, Olefsky J. Improvement in glucose tolerance and insulin resistance in obese subjects treated with troglitazone. N Engl J Med 331: 1188-1193, 1994.
56. Park JB, Touyz RM, Chen X, Schiffrin EL. Chronic treatment with a superoxide dismutase mimetic prevents vascular remodeling and progression of hypertension in salt-loaded stroke-prone spontaneously hypertensive rats. Am J Hypertens 15: 78-84, 2002.
57. Patel A, MacMahon S, Chalmers J, Neal B, Billot L, Woodward M, Marre M, Cooper M, Glasziou P, Grobbee D, Hamet P, Harrap S, Heller S, Liu L, Mancia G, Mogensen CE, Pan C, Poulter N, Rodgers A, Williams B, Bompoint S, de Galan BE, Joshi R, Travert F. Intensive blood glucose control and vascular outcomes in patients with type 2 diabetes. N Engl J Med 358: 2560-2572, 2008.
58. Potashnik R, Bloch-Damti A, Bashan N, Rudich A. IRS1 degradation and increased serine phosphorylation cannot predict the degree of metabolic insulin resistance induced by oxidative stress. Diabetologia 46: 639-648, 2003.
59. Potenza MA, Gagliardi S, Nacci C, Carratù MR, Montagnani M. Endothelial dysfunction in diabetes: from mechanisms to therapeutic targets. Current Medicinal Chemistry 16: 94-112, 2009.
60. Potenza MA, Marasciulo FL, Chieppa DM, Brigiani GS, Formoso G, Quon MJ, Montagnani M. Insulin resistance in spontaneously hypertensive rats is associated with endothelial dysfunction characterized by imbalance between NO and ET-1 production. Am J Physiol Heart Circ Physiol 289: H813-H822, 2005.
61. Potenza MA, Marasciulo FL, Tarquinio M, Quon MJ, Montagnani M. Treatment of spontaneously hypertensive rats with rosiglitazone and/or enalapril restores balance between vasodilator and vasoconstrictor actions of insulin with simultaneous improvement in hypertension and insulin resistance. Diabetes 55: 3594-3603, 2006.
62. Potenza MA, Marasciulo FL, Tarquinio M, Tiravanti E, Colantuono G, Federici A, Kim JA, Quon MJ, Montagnani M. EGCG, a green tea polyphenol, improves endothelial function and insulin sensitivity, reduces blood pressure, and protects against myocardial I/R injury in SHR. Am J Physiol Endocrinol Metab 292: E1378-E1387, 2007.
63. Qayyum R, Adomaityte J. Meta-analysis of the effect of thiazolidinediones on serum C-reactive protein levels. Am J Cardiol 97: 655-658, 2006.
64. Rebolledo OR, Marra CA, Raschia A, Rodriguez S, Gagliardino JJ. Abdominal adipose tissue: early metabolic dysfunction associated to insulin resistance and oxidative stress induced by an unbalanced diet. Horm Metab Res 40: 794-800, 2008.
65. Sarafidis PA, Lasaridis AN. Actions of peroxisome proliferator-activated receptors-gamma agonists explaining a possible blood pressure-lowering effect. Am J Hypertens 19: 646-653, 2006.
66. Schluter T, Steinbach AC, Steffen A, Rettig R, Grisk O. Apocynin-induced vasodilation involves Rho kinase inhibition but not NADPH oxidase inhibition. Cardiovasc Res 80: 271-279, 2008.
67. Schnackenberg CG, Wilcox CS. Two-week administration of tempol attenuates both hypertension and renal excretion of 8-Iso prostaglandin f2alpha. Hypertension 33: 424-428, 1999.
68. Singh S, Loke YK, Furberg CD. Long-term risk of cardiovascular events with rosiglitazone: a meta-analysis. JAMA 298: 1189-1195, 2007.
69. Srinivasan S, Hatley ME, Bolick DT, Palmer LA, Edelstein D, Brownlee M, Hedrick CC. Hyperglycaemia-induced superoxide production decreases eNOS expression via AP-1 activation in aortic endothelial cells. Diabetologia 47: 1727-1734, 2004.
70. Stuhlinger MC, Abbasi F, Chu JW, Lamendola C, McLaughlin TL, Cooke JP, Reaven GM, Tsao PS. Relationship between insulin resistance and an endogenous nitric oxide synthase inhibitor. JAMA 287: 1420-1426, 2002.
71. Tao L, Liu HR, Gao E, Teng ZP, Lopez BL, Christopher TA, Ma XL, Batinic-Haberle I, Willette RN, Ohlstein EH, Yue TL. Antioxidative, antinitrative, and vasculoprotective effects of a peroxisome proliferator-activated receptor-gamma agonist in hypercholesterolemia. Circulation 108: 2805-2811, 2003.
72. Vallance P, Leiper J. Cardiovascular biology of the asymmetric dimethylarginine: dimethylarginine dimethylaminohydrolase pathway. Arterioscler Thromb Vasc Biol 24: 1023-1030, 2004.
73. Williams HC, Griendling KK. NADPH oxidase inhibitors: new antihypertensive agents? J Cardiovasc Pharmacol 50: 9-16, 2007.
74. Yki-Jarvinen H. Thiazolidinediones. N Engl J Med 351: 1106-1118, 2004.
75. Zalba G, Beaumont FJ, San Jose G, Fortuno A, Fortuno MA, Etayo JC, Diez J. Vascular NADH/NADPH oxidase is involved in enhanced superoxide production in spontaneously hypertensive rats. Hypertension 35: 1055-1061, 2000.
76. Zhao S, Zhang C, Lin Y, Yang P, Yu Q, Chu Y, Yang P, Fan J, Liu E. The effects of rosiglitazone on aortic atherosclerosis of cholesterol-fed rabbits. Thromb Res 123: 281-287, 2008.
77. Zhou X, Bohlen HG, Miller SJ, Unthank JL. NAD(P)H oxidase-derived peroxide mediates elevated basal and impaired flow-induced NO production in SHR mesenteric arteries in vivo. Am J Physiol Heart Circ Physiol 295: H1008-H1016, 2008.